Having partially developed inside caterpillars, the larvae of the wasps manipulate their hosts into watching over them as a mother or bodyguard might.

A team that has done extensive field studies with infected caterpillars say they have the first conclusive proof that the manipulative behaviour of some parasitoids increases their chance of survival.

The parasitoid wasp Glyptapanteles lays its eggs, about 80 at a time, in young geometrid caterpillars. The eggs hatch and the larvae feed on the caterpillar's body fluids. When they are fully developed, they eat through the caterpillar's skin, attach themselves to a nearby branch or leaf and wrap themselves up in a cocoon.

Sticking around

At this point, something remarkable and slightly eerie happens.

The caterpillar, still alive, behaves as though controlled by the cocooned larvae. Instead of going about its usual daily business, it stands arched over the cocoons without moving away or feeding.

"We don't know exactly what kills the caterpillars, but it is fascinating that the moment of death seems to be tuned to the duration of the wasp's pupal stage," says Arne Janssen of the University of Amsterdam.

Bodyguard slave

Janssen and colleagues at the Brazilian Federal University of Viçosa noticed that when they moved a paintbrush towards parasitised caterpillars, the insects would thrash about, apparently in an attempt to protect the cocoons.

It wasn't the first time that parasites have been seen to manipulate the behaviour of their hosts. One parasite, for instance, infects an ant and appears to "convince" it to climb to the tops of blades of grass where it is more likely to be eaten by grazing sheep - which the parasite needs to get into in order to complete its life cycle.

But no-one had yet been able to show that the manipulation was not random and did indeed serve the purpose of the parasite. It could be that, rather than changing their behaviour, the parasites simply choose hosts that have abnormal behaviour.

Laboratory parasites

To test the manipulation hypothesis, Janssen's team allowed wasps to infect caterpillars in a laboratory setting. Once the larvae emerged and formed their cocoons, the researchers separated half the cocoons and the caterpillars. The separated cocoons were attached to a leaf next to an unparasitised caterpillar, which was prevented from moving away by a ring of insect glue around the stem.

When they added a stinkbug, a voracious predator of wasp cocoons, the team found that 17 of the 19 parasitised caterpillars thrashed their heads around in the direction of the bug. More than half the time, this knocked the bug off the branch or made it retreat. Unparasitised caterpillars barely noticed the bug, even when it climbed on top of them.

To see if the behaviour affected the survival of wasp cocoons in the wild, the researchers placed over 400 parasitised caterpillars in guava fruit trees one day before the larvae were due to break through their skin.

Once the larvae had cocooned themselves on the nearby branches, the researchers removed half of their bodyguard caterpillars and watched what happened. The survival rate of "guarded" cocoons was twice as high as that of unguarded cocoons.

Wasps 1 caterpillars 0

"The study is absolutely fascinating," says Frédéric Thomas of the Institute for Research and Development in France. "It is the first documented case of manipulative parasites making the host behave as a true bodyguard to protect the parasite. And the experiments show the behavioural change is beneficial only for the wasp."

Although Janssen and his colleagues do not know how the parasites make the caterpillars change their behaviour, they think that a few larvae in each brood may sacrifice themselves to help their brothers and sisters.

"If we dissect the caterpillars, we find one or two parasitoid larvae have stayed behind, even after the rest of the brood has emerged and formed cocoons," says Janssen.

It could be that the larvae that remain in the host control its behaviour in order to make it protect the rest of the brood.

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